Immunological and non-immunological mechanisms of proteinuria

Minerva Urologica e Nefrologica

Volumn 61, Issue 4, 2009, Pages 385-396

  Braun, N ^a   Grone H J ^b   Schena, F P ^c  

^a UNIVERSITY OF ROSTOCK   (Germany)

^b GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

^c POLICLINICO   (Italy)

Author keywords

Glomerulonephritis; Glomerulosclerosis, focal segmental; Lupus erythematosus, systemic; Proteinuria

Indexed keywords

AUTOANTIBODY; CD2 ASSOCIATED PROTEIN; CYTOKINE; NEPHRIN; OXYGEN RADICAL; PODOCIN; TRANSFORMING GROWTH FACTOR BETA;

ANTIGEN ANTIBODY COMPLEX; BASEMENT MEMBRANE; DIABETIC NEPHROPATHY; GENE MUTATION; HEMODYNAMICS; HUMAN; IMMUNOLOGY; INFLAMMATORY CELL; METABOLIC DISORDER; NONHUMAN; PODOCYTE; PROTEINURIA; REVIEW; URINARY EXCRETION;

GLOMERULAR BASEMENT MEMBRANE; GLOMERULONEPHRITIS, MEMBRANOUS; GLOMERULOSCLEROSIS, FOCAL SEGMENTAL; HUMANS; LUPUS NEPHRITIS; PODOCYTES; PROTEINURIA;

EID: 76349110734     PISSN: 03932249     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Review

References (82)

1. Ludwig CFW. De viribus physicis secretionem urinae. Marburg: Marburgi cattorum typis elwerti academicis; 1842.
2. Smithies O. Why the kidney glomerulus does not clog: a gel permeation/diffiision hypothesis of renal function. Proc Natl Acad Sci U S A 2003;100:4108-13.
3. Ryan GB, Karnovsky MJ. Distribution of endogenous albumin in the rat glomerulus:role of hemodynamic factors in glomerular barrier function. Kidney Int 1976;9:36-45.
4. Tojo A, Endou H. Intrarenal handling of proteins in rats using fractional micropuncture technique. Am J Physiol 1992;263:F601-F606.
5. Russo LM, Bakris GL, Comper WD. Renal handling of albumin:a critical review of basic concepts and perspective. Am J Kidney Dis 2002;39:899-919.
6. Farquhar MG, Palade GE. Glomerular permeability. II. Ferritin transfer across the glomerular capillary wall in nephrotic rats. J Exp Med 1961;114:699-716.
7. Tryggvason K, Patrakka J, Wartiovaara J. Hereditary proteinuria syndromes and mechanisms of proteinuria. N Engl J Med 2006;354:1387-401.
8. Norio R. Heredity in the congenital nephrotic syndrome. A genetic study of 57 finnish families with a review of reported cases. Ann Paediatr Fenn 1966;12:(Suppl 27):1-94.
9. Boute N, Gribouval O, Roselli S, Benessy F, Lee H, Fuchshuber A et al. NPHS2, encoding the glomerular protein podocin, is mutated in autosomal recessive steroid-resistant nephrotic syndrome. Nat Genet 2000;24:349-54.
10. Henderson JM, Alexander MP, Pollak MR. Patients with ACTN4 mutations demonstrate distinctive features of glomerular injury. J Am Soc Nephrol 2009;20:961-8.
11. Reiser J, Polu KR, Moller CC, Kenlan P, Altintas MM, Wei C et al. TRPC6 is a glomerular slit diaphragm-associated channel required for normal renal function. Nat Genet 2005;37:739-44.
12. Shih NY, Li J, Karpitskii V, Nguyen A, Dustin ML, Kanagawa O et al. Congenital nephrotic syndrome in mice lacking CD2-associated protein. Science 1999;286:312-5.
13. Löwik MM, Groenen PJ, Levtchenko EN, Monnens LA, van den Heuvel LP. Molecular genetic analysis of podocyte genes in focal segmental glomerulosclerosis-a review. Eur J Pediatr 2009;168:1291-304.
14. Putaala H, Soininen R, Kilpelainen P, Wartiovaara J, Tryggvason K. The murine nephrin gene is specifically expressed in kidney, brain and pancreas:inactivation of the gene leads to massive proteinuria and neonatal death. Hum Mol Genet 2001;10:1-8.
15. Kestilä M, Lenkkeri U, Mannikko M, Lamerdin J, McCready P, Putaala H et al. Positionally cloned gene for a novel glomerular protein - nephrin - is mutated in congenital nephrotic syndrome Mol Cell 1998;1:575-82.
16. Laine J, Jalanko H, Holthofer H, Krogerus L, Rapola J, von WE, Lautenschlager I, Salmela K, Holmberg C. Post-transplantation nephrosis in congenital nephrotic syndrome of the Finnish type. Kidney Int 1993;44:867-74.
17. Harita Y, Kurihara H, Kosako H, Tezuka T, Sekine T, Igarashi T et al. Neph1, a component of the kidney slit diaphragm, is tyrosine- phosphorylated by the Src family tyrosine kinase and modulates intracellular signaling by binding to Grb2. J Biol Chem 2008;283:9177-86.
18. Sellin L, Huber TB, Gerke P, Quack I, Pavenstadt H, Walz G. NEPH1 defines a novel family of podocin interacting proteins. FASEB J 2003;17:115-7.
19. Garg P, Verma R, Nihalani D, Johnstone DB, Holzman LB. Neph1 cooperates with nephrin to transduce a signal that induces actin polymerization. Mol Cell Biol 2007;27:8698-712.
20. Ihalmo P, Schmid H, Rastaldi MP, Mattinzoli D, Langham RG, Luimula P et al. Expression of filtrin in human glomerular diseases. Nephrol Dial Transplant 2007;22:1903-9.
21. Gerke P, Sellin L, Kretz O, Petraschka D, Zentgraf H, Benzing T et al. Walz G. NEPH2 is located at the glomerular slit diaphragm, interacts with nephrin and is cleaved from podocytes by metalloproteinases. J Am Soc Nephrol 2005;16:1693-702.
22. Kaplan JM, Kim SH, North KN, Rennke H, Correia LA, Tong HQ et al. Mutations in ACTN4, encoding alpha-actinin-4, cause familial focal segmental glomerulosclerosis. Nat Genet 2000;24:251-6.
23. McKenzie LM, Hendrickson SL, Briggs WA, Dart RA, Korbet SM, Mokrzycki MH et al. NPHS2 variation in sporadic focal segmental glomerulosclerosis. J Am Soc Nephrol 2007;18:2987-95.
24. Hildebrandt F, Heeringa SF. Specific podocin mutations determine age of onset of nephrotic syndrome all the way into adult life. Kidney Int 2009;75:669-71.
25. Koziell A, Grech V, Hussain S, Lee G, Lenkkeri U, Tryggvason K et al. Genotype/phenotype correlations of NPHS1 and NPHS2 mutations in nephrotic syndrome advocate a functional inter-relationship in glomerular filtration. Hum Mol Genet 2002;11:379-88.
26. Machuca E, Hummel A, Nevo F, Dantal J, Martinez F, Al-Sabban E et al. Clinical and epidemiological assessment of steroid-resistant nephrotic syndrome associated with the NPHS2 R229Q variant. Kidney Int 2009;75:727-35.
27. Tanoue T, Takeichi M. New insights into Fat Cadherins. J Cell Sci 2005;118:2347-53.
28. Tanoue T, Takeichi M. Mammalian Fat1 Cadherin regulates actin dynamics and cell-cell contact. J Cell Biol 2004;165:517-28.
29. Moeller MJ, Soofi A, Braun GS, Li X, Watzl C, Kriz W, Holzman LB. Protocadherin FAT1 binds Ena/VASP proteins and is necessary for actin dynamics and cell polarization EMBO. J 2004;23:3769-79.
30. Ciani L, Patel A, Allen ND, ffrench-Constant C. Mice lacking the giant protocadherin mFAT1 exhibit renal slit junction abnormalities and a partially penetrant cyclopia and anophthalmia phenotype. Mol Cell Biol 2003;23:3575-82.
31. Inoue T, Yaoita E, Kurihara H, Shimizu F, Sakai T, Kobayashi T et al. FAT is a component of glomerular slit diaphragms. Kidney Int 2001;59:1003-12.
32. Dustin ML, Olszowy MW, Holdorf AD, Li J, Bromley S, Desai N et al. A novel adaptor protein orchestrates receptor patterning and cytoskeletal polarity in T-cell contacts Cell 1998;94:667-77.
33. Kim JM, Wu H, Green G, Winkler CA, Kopp JB, Miner JH et al. CD2-associated protein haploinsufficiency is linked to glomerular disease susceptibility. Science 2003;300:1298-300.
34. Welsch T, Endlich N, Gokce G, Doroshenko E, Simpson JC, Kriz W et al. of CD2AP with dynamic actin on vesicles in podocytes. Am J Physiol Renal Physiol 2005;289:F1134-F1143.
35. Asanuma K, Campbell KN, Kim K, Faul C, Mundel P. Nuclear relocation of the nephrin and CD2AP-binding protein dendrin promotes apoptosis of podocytes. Proc Natl Acad Sci U S A 2007;104:10134-9.
36. Schiffer M, Mundel P, Shaw AS, Bottinger EP. A novel role for the adaptor molecule CD2-associated protein in transforming growth factor-beta-induced apoptosis. J Biol Chem 2004;279:37004-12.
37. Huber TB, Kwoh C, Wu H, Asanuma K, Godel M, Hartleben B et al. Bigenic mouse models of focal segmental glomerulosclerosis involving pairwise interaction of CD2AP, Fyn, and synaptopodin. J Clin Invest 2006;116:1337-45.
38. Faul C, Donnelly M, Merscher-Gomez S, Chang YH, Franz S, Delfgaauw J et al. The actin cytoskeleton of kidney podocytes is a direct target of the antiproteinuric effect of cyclosporine. A Nat Med 2008;14:931-8.
39. Ghiggeri GM, Dagnino M, Parodi S, Zennaro C, Amoroso A, Pugliese F et al. Discordant evolution of nephrotic syndrome in mono- and dizygotic twins Pediatr Nephrol 2006;21:419-22.
40. Kerjaschki D, Farquhar MG. The pathogenic antigen of Heymann nephritis is a membrane glycoprotein of the renal proximal tubule brush border. Proc Natl Acad Sci U S A 1982;79:5557-61.
41. Tramontano A, Makker SP. Conformation and glycosylation of a megalin fragment correlate with nephritogenicity in Heymann nephritis. J Immunol 2004;172:2367-73.
42. Ronco P, Debiec H. Target antigens and nephritogenic antibodies in membranous nephropathy:of rats and men. Semin Immunopathol 2007;29:445-58.
43. Beck LH, Jr., Bonegio RG, Lambeau G, Beck DM, Powell DW, Cummins TD et al. M-type phospholipase A2 receptor as target antigen in idiopathic membranous nephropathy. N Engl J Med 2009;361:11-21.
44. Wu CC, Chen JS, Lin SH, Chen A, Sytwu HK, Lin YF. Experimental model of membranous nephropathy in mice:sequence of histological and biochemical events. Lab Anim 2008;42:350-9.
45. Couser WG. Pathogenesis of glomerular damage in glomerulonephritis. Nephrol Dial Transplant 1998;13(Suppl 1):10-5.
46. Spicer ST, Tran GT, Killingsworth MC, Carter N, Power DA, Paizis K et al. Induction of passive Heymann nephritis in complement component 6-deficient PVG rats. J Immunol 2007;179:172-8.
47. Barnes JL, Reznicek MJ, Radnik RA, Venkatachalam MA. Anionization of an antigen promotes glomerular binding and immune complex formation. Kidney Int 1988;34:156-63.
48. Batsford SR, Mihatsch MJ, Rawiel M, Schmiedeke TM, Vogt A. Surface charge distribution is a determinant of antigen deposition in the renal glomerulus:studies employing 'charge-hybrid' molecules. Clin Exp Immunol 1991;86:471-7.
49. McBurney WT, Lendemans DG, Myschik J, Hennessy T, Rades T, Hook S. In vivo activity of cationic immune stimulating complexes (PLUSCOMs). Vaccine 2008;26:4549-56.
50. Bento-Abreu A, Velasco A, Polo-Hernandez E, Lillo C, Kozyraki R, Tabernero A et al. Albumin endocytosis via megalin in astrocytes is caveola- and Dab-1 dependent and is required for the synthesis of the neurotrophic factor oleic acid.J Neurochem 2009;111:49-60.
51. Christensen EI, Verroust PJ, Nielsen R. Receptor-mediated endocytosis in renal proximal tubule. Pflugers Arch 2009;458:1039-48.
52. Rock KL. A new foreign policy:MHC class I molecules monitor the outside world. Immunol Today 1996;17:131-7.
53. Coers W, Brouwer E, Vos JT, Chand A, Huitema S, Heeringa P et al. Podocyte expression of MHC class I and II and intercellular adhesion molecule-1 (ICAM-1) in experimental pauci-immune crescentic glomerulonephritis. Clin Exp Immunol 1994;98:279-86.
54. Wu H, Zhang GY, Knight JF. T cell lines specific for a synthetic Heymann nephritis peptide derived from the receptor-associated protein. Clin Exp Immunol 2000;121:157-64.
55. Neale TJ, Ojha PP, Exner M, Poczewski H, Ruger B, Witztum JL et al. Proteinuria in passive Heymann nephritis is associated with lipid peroxidation and formation of adducts on type IV collagen. J Clin Invest 1994;94:1577-84.
56. Markowitz GS, D'Agati VD. Classification of lupus nephritis. Curr Opin Nephrol Hypertens 2009;18:220-5.
57. Blank M, Shoenfeld Y. The story of the 16/6 idiotype and systemic lupus erythematosus. Isr Med Assoc J 2008;10:37-9.
58. Mjelle JE, Kalaaji M, Rekvig OP. Exposure of chromatin and not high affinity for dsDNA determines the nephritogenic impact of anti-dsDNA antibodies in (NZBxNZW)F1 mice. Autoimmunity 2009;42:104-11.
59. Perez de LG, Maier H, Franz TJ, Escribese M, Chilla S, Segerer S et al. Chemokine receptor Ccr2 deficiency reduces renal disease and prolongs survival in MRL/lpr lupus-prone mice. J Am Soc Nephrol 2005;16:3592-601.
60. Pawar RD, Patole PS, Zecher D, Segerer S, Kretzler M, Schlondorff D et al. Toll-like receptor-7 modulates immune complex glomerulonephritis. J Am Soc Nephrol 2006;17:141-9.
61. Tucci M, Barnes EV, Sobel ES, Croker BP, Segal MS, Reeves WH et al. Strong association of a functional polymorphism in the monocyte chemoattractant protein 1 promoter gene with lupus nephritis. Arthritis Rheum 2004;50:1842-9.
62. Couzi L, Merville P, Deminiere C, Moreau JF, Combe C, Pellegrin JL et al. Predominance of CD8+ T lymphocytes among periglomerular infiltrating cells and link to the prognosis of class III and class IV lupus nephritis. Arthritis Rheum 2007;56:2362-70.
63. Kurts C, Heymann F, Lukacs-Kornek V, Boor P, Floege J. Role of T cells and dendritic cells in glomerular immunopathology. Semin Immunopathol 2007;29:317-35.
64. Heymann F, Meyer-Schwesinger C, Hamilton-Williams EE, Hammerich L, Panzer U, Kaden S et al. Kidney dendritic cell activation is required for progression of renal disease in a mouse model of glomerular injury. J Clin Invest 2009;119:1286-97.
65. Igawa T, Nakashima H, Sadanaga A, Masutani K, Miyake K, Shimizu S et al. Deficiency in EBV-induced gene 3 (EBI3) in MRL/lpr mice results in pathological alteration of autoimmune glomerulonephritis and sialadenitis. Mod Rheumatol 2009;19:33-41.
66. Artero ML, Sharma R, Savin VJ, Vincenti F. Plasmapheresis reduces proteinuria and serum capacity to injure glomeruli in patients with recurrent focal glomerulosclerosis. Am J Kidney Dis 1994;23:574-81.
67. Dantal J, Bigot E, Bogers W, Testa A, Kriaa F, Jacques Y et al. Effect of plasma protein adsorption on protein excretion in kidney-transplant recipients with recurrent nephrotic syndrome. N Engl J Med 1994;330:7-14.
68. Lagrue G, Xheneumont S, Branellec A, Hirbec G, Weil B. A vascular permeability factor elaborated from lymphocytes. I. Demonstration in patients with nephrotic syndrome. Biomedicine 1975;23:37-40.
69. Lagrue G, Branellec A, Blanc C. A vascular permeability factor in lymphocyte culture supernantants from patients with nephrotic syndrome. II. Pharmacological and physiochemical properities. Biomedicine 1975;23:73-5.
70. Savin VJ, Sharma R, Sharma M, McCarthy ET, Swan SK, Ellis E et al. Circulating factor associated with increased glomerular permeability to albumin in recurrent focal segmental glomerulosclerosis. N Engl J Med 1996;334:878-83.
71. Kondo S, Yoshizawa N, Kusumi Y, Takeuchi A, Torikata C. Studies of glomerular permeability factor (GPF) in focal segmental glomerular sclerosis and the relationship between GPF and vascular permeability factor (VPF). Clin Nephrol 1999;52:278-84.
72. Coward RJ, Foster RR, Patton D, Ni L, Lennon R, Bates DO et al. Nephrotic plasma alters slit diaphragm-dependent signaling and translocates nephrin, Podocin, and CD2 associated protein in cultured human podocytes. J Am Soc Nephrol 2005;16:629-37.
73. Lennon R, Singh A, Welsh GI, Coward RJ, Satchell S, Ni L et al. Hemopexin induces nephrin-dependent reorganization of the actin cytoskeleton in podocytes. J Am Soc Nephrol 2008;19:2140-9.
74. Fodor P, Saitua MT, Rodriguez E, Gonzalez B, Schlesinger L. T-cell dysfunction in minimal change nephrotic syndrome of childhood. Am J Dis Child 1982;136:713-7.
75. Shalhoub RJ. Pathogenesis of lipoid nephrosis: a disorder of T-cell function. Lancet 1974;2:556-60.
76. Meyrier AY. Treatment of focal segmental glomerulosclerosis with immunophilin modulation: when did we stop thinking about pathogenesis? Kidney Int 2009;76:487-91.
77. Palmer SC, Nand K, Strippoli GF. Interventions for minimal change disease in adults with nephrotic syndrome. Cochrane Database Syst Rev 2008;CD001537.
78. Braun N, Schmutzler F, Lange C, Perna A, Remuzzi A, Risler T et al. Immunosuppressive treatment for focal segmental glomerulosclerosis in adults (Review). Cochrane Database Syst Re 2008;CD003233, 2008.
79. Bao L, Haas M, Pippin J, Wang Y, Miwa T, Chang A et al. Focal and segmental glomerulosclerosis induced in mice lacking decay-accelerating factor in T cells. J Clin Invest 2009;119:1264-74.
80. Koya D, Haneda M, Nakagawa H, Isshiki K, Sato H, Maeda S et al. Amelioration of accelerated diabetic mesangial expansion by treatment with a PKC beta inhibitor in diabetic db/db mice, a rodent model for type 2 diabetes. FASEB J 2000;14:439-447.
81. Doublier S, Salvidio G, Lupia E, Ruotsalainen V, Verzola D. Deferrari G et al. Nephrin expression is reduced in human diabetic nephropathy:evidence for a distinct role for glycated albumin and angiotensin II. Diabetes 2003;52:1023-30.
82. Pagtalunan ME, Miller PL, Jumping-Eagle S, Nelson RG, Myers BD, Rennke HG et al. Podocyte loss and progressive glomerular injury in type II diabetes J Clin Invest 1997;99:342-8.